Skip to main content Accessibility help

Paternal effects correlate with female reproductive stimulation in the polyandrous ladybird Cheilomenes sexmaculata

  • M.A. Mirhosseini (a1), J.P. Michaud (a2), M.A. Jalali (a1) and M. Ziaaddini (a1)

Components of male seminal fluids are known to stimulate fecundity and fertility in females of numerous insect species and paternal effects on offspring phenotype are also known, but no studies have yet demonstrated links between male effects on female reproduction and those on progeny phenotype. In separate laboratory experiments employing 10-day-old virgin females of Cheilomenes sexmaculata (F.), we varied male age and mating history to manipulate levels of male allomones and found that the magnitude of paternal effects on progeny phenotype was correlated with stimulation of female reproduction. Older virgin males remained in copula longer than younger ones, induced higher levels of female fecundity, and sired progeny that developed faster to yield heavier adults. When male age was held constant (13 days), egg fertility declined as a function of previous male copulations, progeny developmental times increased, and the adult weight of daughters declined. These results suggest that male epigenetic effects on progeny phenotype act in concert with female reproductive stimulation; both categories of effects increased as a consequence of male celibacy (factor accumulation), and diminished as a function of previous matings (factor depletion). Male factors that influence female reproduction are implicated in sexual conflict and parental effects may extend this conflict to offspring phenotype. Whereas mothers control the timing of oviposition events and can use maternal effects to tailor progeny phenotypes to prevailing or anticipated conditions, fathers cannot. Since females remate and dilute paternity in polyandrous systems, paternal fitness will be increased by linking paternal effects to female fecundity stimulation, so that more benefits accrue to the male's own progeny.

Corresponding author
* Author for correspondence Phone: 785-625-3425 Fax: 785-623-4369 Email:
Hide All
Adler, M.I. & Bonduriansky, R. (2013) Paternal effects on offspring fitness reflect father's social environment. Evolutionary Biology 40, 288292.
Avila, F.W., Sirot, L.K., LaFlamme, B.A., Rubinstein, C.D. & Wolfner, M.F. (2011) Insect seminal fluid proteins: identification and function. Annual Review of Entomology 56, 2140.
Bind, R.B. (2007) Reproductive behaviour of a generalist aphidophagous ladybird beetle, Cheilomenes sexmaculata . International Journal of Tropical Insect Science 27, 7884.
Bonduriansky, R. & Head, M. (2007) Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae). Journal of Evolutionary Biology 20, 23792388.
Brown, W.D., Crespi, B.J. & Choe, J.C. (1997) Sexual conflict and the evolution of mating systems. pp. 352377 in Choe, J.C. & Crespi, B.J. (Eds) The Evolution of Mating Systems in Insects and Arachnids. Cambridge, UK, Cambridge University Press.
Chen, P.S., Strumm-Zollinger, E., Aigaki, T., Balmer, J., Bienz, M. & Bohlen, P. (1988) A male accessory gland peptide that regulates reproductive behavior of female Drosophila melanogaster . Cell 54, 291298.
Eberhard, W.G. (1996) What is cryptic female choice? pp. 443 in Eberhard, W.G. (Ed.) Female Control: Sexual Selection by Cryptic Female Choice. Princeton, New Jersey, Princeton University Press.
Eberhard, W.G. (1997) Sexual selection by cryptic female choice in insects and arachnids. pp 3257 in Choe, J.C. & Crespi, B.J. (Eds) The Evolution of Mating Systems in Insects and Arachnids. Cambridge, UK, Cambridge University Press.
Gillott, C. (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annual Review of Entomology 48, 163184.
Gioti, A., Wigby, S., Wertheim, B., Schuster, E., Martinez, P., Pennington, C.J., Partridge, L. & Chapman, T. (2012) Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females. Proceedings of the Royal Society of London, Series B 279, 44234432.
Hanin, O., Azrielli, A., Applebaum, S.W. & Rafaeli, A. (2012) Functional impact of silencing the Helicoverpa armigera sex-peptide receptor on female reproductive behaviour. Insect Molecular Biology 21, 161167.
Hunt, J. & Simmons, L.W. (2000) Maternal and paternal effects on offspring phenotype in the dung beetle Onthophagus taurus . Evolution 54, 936941.
Majerus, M.E.N. (1994) Female promiscuity maintains high fertility in ladybirds (Coleoptera: Coccinellidae). Entomologist's Monthly Magazine 130, 205209.
Michaud, J.P. & Qureshi, J.A. (2006) Reproductive diapause in Hippodamia convergens (Coleoptera: Coccinellidae) and its life history consequences. Biological Control 39, 193200.
Michaud, J.P., Bista, M., Mishra, G. & Singh, O. (2013) Sexual activity diminishes male virility in two Coccinella species: consequences for female fertility and progeny development. Bulletin of Entomological Research 103, 570577.
Miller, P.M., Gavrilet, S. & Rice, W.R. (2006) Sexual conflict via maternal-effect genes in ZW species. Science 312, 73.
Mishra, G. & Omkar, (2006) Ageing trajectory and longevity trade-off in an aphidophagous ladybird, Propylea dissecta (Coleoptera: Coccinellidae). European Journal of Entomology 103, 3340.
Mousseau, T.A. & Dingle, H. (1991) Maternal effects in insect life histories. Annual Review of Entomology 36, 511534.
Mousseau, T.A. & Fox, C.W. (1998) Maternal Effects as Adaptations. New York, USA, Oxford University Press.
Mousseau, T.A., Uller, T., Wapstra, E. & Badyaev, A.V. (2009) Evolution of maternal effects: past and present. Philosophical Transactions of the Royal Society of London, Series B, 364, 10351038.
Obata, S. (1987) Mating behavior and sperm transfer in the ladybird beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Applied Entomology and Zoology 22, 434442.
Omkar, & Mishra, G. (2005) Evolutionary significance of promiscuity in an aphidophagous ladybird, Propylea dissecta . Bulletin of Entomological Research 95, 527533.
Omkar, & Pervez, A. (2005) Mating behaviour of an aphidophagous ladybird beetle, Propylea dissecta (Mulsant). Insect Science 12, 3744.
Omkar, & Singh, S.K. (2009) Effect of parental ageing on offspring developmental and survival attributes in an aphidophagous ladybird, Cheilomenes sexmaculata . Journal of Applied Entomology 133, 500504.
Omkar, , Mishra, G. & Singh, S.K. (2006 a) Optimal number of matings in two aphidophagous ladybirds. Ecological Entomology 31, 114.
Omkar, , Singh, S.K. & Singh, K. (2006 b) Effect of age on reproductive attributes of an aphidophagous ladybird, Cheilomenes sexmaculata . Insect Science 13, 301308.
Omkar, , Singh, S.K. & Mishra, G. (2010) Parental age at mating affects reproductive attributes of the aphidophagous ladybird beetle, Coelophora saucia (Coleoptera: Coccinellidae). European Journal of Entomology 107, 341347.
Omkar, , Sahu, J. & Kumar, G. (2013) Age specific mating incidence and reproductive behavior of the ladybird beetle, Anegleis cardoni (Weise) (Coleoptera: Coccinellidae). Journal of Asia-Pacific Entomology 16, 263268.
Qvarnstrom, A. & Price, T.D. (2001) Maternal effects, paternal effects and sexual selection. Trends in Ecology and Evolution 16, 95100.
Semyanov, V.P. (1970) Biological properties of Adalia bibunctata L. (Coleoptera: Coccinellidae) in conditions of Leningrad region. Zashchita Rastenii ot Vreditelei i Boleznei 127, 105112 (in Russian).
Shea, N., Pen, I. & Uller, T. (2011) Three epigenetic information channels and their different roles in evolution. Journal of Evolutionary Biology 24, 11781187.
Simmons, L.W. & Garcia-Gonzalez, F. (2007) Female crickets trade offspring viability for fecundity. Journal of Evolutionary Biology 20, 16171623.
SPSS (2006) Version 15.0. Chicago, Illinois, SPSS Inc.
Srivastava, S. & Omkar, (2004) Age-specific mating and reproductive senescence in the seven-spotted ladybird, Coccinella septempunctata . Journal of Applied Entomology 128, 452458.
Tregenza, T. & Wedell, N. (2002) Polyandrous females avoid costs of inbreeding. Nature 415, 7173.
Vargas, G.A., Michaud, J.P. & Nechols, J.R. (2012 a) Cryptic maternal effects in Hippodamia convergens vary with maternal age and body size. Entomologia Experimentalis et Applicata 146, 302311.
Vargas, G.A., Michaud, J.P. & Nechols, J.R. (2012 b) Maternal effects shape dynamic trajectories of reproductive allocation in the ladybird Coleomegilla maculata . Bulletin of Entomological Research 102, 558565.
Wedell, N., Kvarnemo, C., Lessells, M. & Tregenza, T. (2006) Sexual conflict and life histories. Animal Behaviour 71, 9991011.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Bulletin of Entomological Research
  • ISSN: 0007-4853
  • EISSN: 1475-2670
  • URL: /core/journals/bulletin-of-entomological-research
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed